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Chen J, Zhang W, Bao J, Wang K, Zhao Q, Zhu Y, Chen Y. Implications of ultrasound-based deep learning model for preoperatively differentiating combined hepatocellular-cholangiocarcinoma from hepatocellular carcinoma and intrahepatic cholangiocarcinoma. Abdom Radiol (NY) 2024; 49:93-102. [PMID: 37999743 DOI: 10.1007/s00261-023-04089-4] [Citation(s) in RCA: 3] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/22/2023] [Revised: 10/08/2023] [Accepted: 10/09/2023] [Indexed: 11/25/2023]
Abstract
OBJECTIVES The current study developed an ultrasound-based deep learning model to make preoperative differentiation among hepatocellular carcinoma (HCC), intrahepatic cholangiocarcinoma (ICC), and combined hepatocellular-cholangiocarcinoma (cHCC-ICC). METHODS The B-mode ultrasound images of 465 patients with primary liver cancer were enrolled in model construction, comprising 264 HCCs, 105 ICCs, and 96 cHCC-ICCs, of which 50 cases were randomly selected to form an independent test cohort, and the rest of study population was assigned to a training and validation cohorts at the ratio of 4:1. Four deep learning models (Resnet18, MobileNet, DenseNet121, and Inception V3) were constructed, and the fivefold cross-validation was adopted to train and validate the performance of these models. The following indexes were calculated to determine the differential diagnosis performance of the models, including sensitivity, specificity, accuracy, positive predictive value (PPV), negative predictive value (NPV), F-1 score, and area under the receiver operating characteristic curve (AUC) based on images in the independent test cohort. RESULTS Based on the fivefold cross-validation, the Resnet18 outperformed other models in terms of accuracy and robustness, with the overall training and validation accuracy as 99.73% (± 0.07%) and 99.35% (± 0.53%), respectively. Furthers validation based on the independent test cohort suggested that Resnet 18 yielded the best diagnostic performance in identifying HCC, ICC, and cHCC-ICC, with the sensitivity, specificity, accuracy, PPV, NPV, F1-score, and AUC of 84.59%, 92.65%, 86.00%, 85.82%, 92.99%, 92.37%, 85.07%, and 0.9237 (95% CI 0.8633, 0.9840). CONCLUSION Ultrasound-based deep learning algorithm appeared a promising diagnostic method for identifying cHCC-ICC, HCC, and ICC, which might play a role in clinical decision making and evaluation of prognosis.
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Affiliation(s)
- Jianan Chen
- The First Affiliated Hospital of Guangdong Pharmaceutical University, Guangzhou, Guangdong, China
| | - Weibin Zhang
- Department of Ultrasound, Huashan Hospital, Fudan University, Shanghai, China
| | - Jingwen Bao
- School of Medical Science, Hexi University, Zhangye, China
| | - Kun Wang
- Department of Ultrasound, The Affiliated Hospital of Binzhou Medical University, Binzhou, China
| | - Qiannan Zhao
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
| | - Yuli Zhu
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China.
| | - Yanling Chen
- Department of Radiology, The First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, Guangdong, China.
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China.
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Lv TR, Hu HJ, Ma WJ, Liu F, Jin YW, Li FY. Meta-analysis of prognostic factors for overall survival and disease-free survival among resected patients with combined hepatocellular carcinoma and cholangiocarcinoma. EUROPEAN JOURNAL OF SURGICAL ONCOLOGY 2024; 50:107279. [PMID: 38000116 DOI: 10.1016/j.ejso.2023.107279] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/14/2023] [Revised: 11/09/2023] [Accepted: 11/15/2023] [Indexed: 11/26/2023]
Abstract
BACKGROUND Combined hepatocellular carcinoma and cholangiocarcinoma (CHCC-CC) is a rare subtype of primary liver malignancy and has been treated equally as intra-hepatic cholangiocarcinoma (IHCC) according to the 8th AJCC staging system. Owing to its rarity, its prognostic factors have been rarely explored and defined. METHODS PubMed, EMBASE, the Cochrane Library and Web of Science were searched up till January 1st, 2023 and eligible studies were restricted to studies reported prognostic factors of resected CHCC-CC. Standard Parmar modifications were used to determine pooled univariable hazard ratios (HRs). RESULTS A total of eleven studies with 1286 patients with resected classical CHCC-CC were finally included. Pooled results indicated that serum tumor biomarkers, including AFP, CA199, and CEA, were prognostic factors for postoperative overall survival (OS) and disease-free survival (DFS). Moreover, liver cirrhosis (P = 0.010), HBV infection (P = 0.030), and HCV infection (P < 0.001) were prognostic factors for OS. Age (HR = 1.03, P = 0.005) was a prognostic factor for DFS. Tumor size (OS: HR = 2, P < 0.001, DFS: HR = 2.15, P < 0.001), tumor number (OS: HR = 2.05, P < 0.001; DFS: HR = 1.96, P = 0.006), surgical margin (OS: HR = 2.33, <0.001001; DFS: HR = 2.35, P < 0.001), node metastasis (OS: HR = 2.96, P < 0.001; DFS: HR = 2.1, P < 0.001), vascular invasion (OS: HR = 2.17, P < 0.001; DFS: HR = 2.64, P < 0.001), and postoperative prophylactic trans-arterial chemotherapy embolization (PPTACE) (OS: HR = 1.67, P = 0.04; DFS: HR = 2.31, P < 0.001) were common prognostic factors for OS and DFS. CONCLUSION Various risk factors unmentioned in the 8th AJCC staging system were identified. These promising findings would facilitate a more personalized predictive model and help clinicians to stratify patients with different survival outcomes.
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Affiliation(s)
- Tian-Run Lv
- Department of Biliary Tract Surgery, General Surgrey, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan Province, China
| | - Hai-Jie Hu
- Department of Biliary Tract Surgery, General Surgrey, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan Province, China
| | - Wen-Jie Ma
- Department of Biliary Tract Surgery, General Surgrey, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan Province, China
| | - Fei Liu
- Department of Biliary Tract Surgery, General Surgrey, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan Province, China
| | - Yan-Wen Jin
- Department of Biliary Tract Surgery, General Surgrey, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan Province, China
| | - Fu-Yu Li
- Department of Biliary Tract Surgery, General Surgrey, West China Hospital, Sichuan University, Chengdu, 610041, Sichuan Province, China.
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Mi S, Hou Z, Qiu G, Jin Z, Xie Q, Huang J. Liver transplantation versus resection for patients with combined hepatocellular cholangiocarcinoma: A retrospective cohort study. Heliyon 2023; 9:e20945. [PMID: 37876459 PMCID: PMC10590945 DOI: 10.1016/j.heliyon.2023.e20945] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/25/2023] [Revised: 09/29/2023] [Accepted: 10/11/2023] [Indexed: 10/26/2023] Open
Abstract
Background Combined hepatocellular cholangiocarcinoma (CHC) is a rare primary liver cancer, and whether liver transplantation should be implemented among CHC patients is still controversial. We intend to conduct a retrospective cohort study based on the Surveillance, Epidemiology, and End Results (SEER) database to investigate the prognosis of liver transplantation vs. liver resection among CHC patients. Methods Patients diagnosed with CHC (ICD-O-3:8180/3) and treated with transplantation or hepatectomy were extracted from the SEER database (2000-2018). We utilized Propensity Score Matching to control confounding bias. Kaplan-Meier curve was used for survival analysis, and Cox regression was used to find independent factors associated with prognosis. Results We identified 123 (transplantation: 49; resection: 74) patients with CHC who were treated between 2004 and 2015. In the entire cohort, survival analysis demonstrated transplantation group was associated with better overall survival and cancer-specific survival (log-rank p = 0.004 and p = 0.003, respectively). In addition, liver transplantation still conferred better overall and cancer-specific survival than liver resection after Propensity Score Matching (log-rank p = 0.024 and p = 0.048, respectively). However, this advantage didn't appear in the subgroup, regardless of whether the tumor size was greater than 3 cm or not. (≤3 cm: OS log-rank p = 0.230, CSS log-rank p = 0.370; >3 cm: OS log-rank p = 0.110, CSS log-rank p = 0.084). Multivariate analysis validated the finding that liver transplantation was a protective factor for overall survival (HR = 0.55 [0.31-0.95], p = 0.032). Conclusions Liver transplantation may be an option in individuals with CHC and should be taken into consideration due to its advantages in terms of overall survival and cancer-specific survival. However, a sizable sample is required for future studies to determine which subset of CHC patients may benefit more from liver transplantation.
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Affiliation(s)
| | | | - Guoteng Qiu
- Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu, China
| | - Zhaoxing Jin
- Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu, China
| | - Qingyun Xie
- Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu, China
| | - Jiwei Huang
- Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu, China
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Surgical Strategies for Combined Hepatocellular-Cholangiocarcinoma (cHCC-CC). Cancers (Basel) 2023; 15:cancers15030774. [PMID: 36765731 PMCID: PMC9913263 DOI: 10.3390/cancers15030774] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/31/2022] [Revised: 01/17/2023] [Accepted: 01/19/2023] [Indexed: 01/28/2023] Open
Abstract
Combined hepatocellular-cholangiocarcinoma (cHCC-CC) is a tumor entity presenting features of hepatocellular and cholangiocellular epithelial differentiation. Due to the likeness between cHCC-CC, HCC and CC, accurate pretherapeutical diagnosis is challenging and advanced stages are prevalent. Radical oncological surgery is the only curative therapeutical option in patients with cHCC-CC. To reach this goal a profound understanding of this rare liver tumor is crucial. Factors such as clinicopathological characteristics, growth patterns and biological behavior are of central importance. To explore onco-surgical strategies and aspects for complete resection of cHCC-CC and to answer important key questions, an extensive review of the literature was conducted to answer the following questions: What are the best surgical options? Is there a significance for nonanatomical resections? Is there a prognostic value of concomitant lymphadenectomy? What about multimodal concepts in local advanced cHCC-CC? The role of minimally invasive liver surgery (MILS) including the role of robotic liver surgery for cHCC-CC will be discussed. While liver transplantation (LT) is standard for patients with unresectable HCC, the role of LT in cHCC-CC patients is still controversial. How can patients with high risk for early tumor recurrence be identified to avoid aggressive surgical treatment without clinical benefit? The comprehensive understanding of this challenging liver tumor will help to improve future treatment options for these patients.
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Brandão ABDM, Rodriguez S, Fleck Jr ADM, Marroni CA, Wagner MB, Hörbe A, Fernandes MV, Cerski CTS, Coral GP. Propensity-matched analysis of patients with intrahepatic cholangiocarcinoma or mixed hepatocellular-cholangiocarcinoma and hepatocellular carcinoma undergoing a liver transplant. World J Clin Oncol 2022; 13:688-701. [PMID: 36160465 PMCID: PMC9476608 DOI: 10.5306/wjco.v13.i8.688] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/08/2022] [Revised: 06/14/2022] [Accepted: 07/11/2022] [Indexed: 11/08/2022] Open
Abstract
BACKGROUND Cholangiocarcinoma (CC) is a rare tumor that arises from the epithelium of the bile ducts. It is classified according to anatomic location as intrahepatic, perihilar, and distal. Intrahepatic CC (ICC) is rare in patients with cirrhosis due to causes other than primary sclerosing cholangitis. Mixed hepatocellular carcinoma-CC (HCC-CC) is a rare neoplasm that shows histologic findings of both HCC and ICC within the same tumor mass. Due to the difficulties in arriving at the correct diagnosis, patients eventually undergo liver transplantation (LT) with a presumptive diagnosis of HCC on imaging when, in fact, they have ICC or HCC-CC.
AIM To evaluate the outcomes of patients with intrahepatic cholangiocarcinoma or mixed hepatocellular-cholangiocarcinoma on pathological examination after liver transplant.
METHODS Propensity score matching was used to analyze tumor recurrence (TR), overall mortality (OM), and recurrence-free survival (RFS) in LT recipients with pathologically confirmed ICC or HCC-CC matched 1:8 to those with HCC. Progression-free survival and overall mortality rates were computed with the Kaplan-Meier method using Cox regression for comparison.
RESULTS Of 475 HCC LT recipients, 1.7% had the diagnosis of ICC and 1.5% of HCC-CC on pathological examination of the explant. LT recipients with ICC had higher TR (46% vs 11%; P = 0.006), higher OM (63% vs 23%; P = 0.002), and lower RFS (38% vs 89%; P = 0.002) than those with HCC when matched for pretransplant tumor characteristics, as well as higher TR (46% vs 23%; P = 0.083), higher OM (63% vs 35%; P = 0.026), and lower RFS (38% vs 59%; P = 0.037) when matched for posttransplant tumor characteristics. Two pairings were performed to compare the outcomes of LT recipients with HCC-CC vs HCC. There was no significant difference between the outcomes in either pairing.
CONCLUSION Patients with ICC had worse outcomes than patients undergoing LT for HCC. The outcomes of patients with HCC-CC did not differ significantly from those of patients with HCC.
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Affiliation(s)
- Ajacio Bandeira de Mello Brandão
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre 90050170, RS, Brazil
- Liver Transplantation Group, Santa Casa de Misericórdia de Porto Alegre, Porto Alegre 90020090, RS, Brazil
| | - Santiago Rodriguez
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre 90050170, RS, Brazil
- Department of Hepatology, Hospital Vozandes Quito-HVQ, Quito 170521, Ecuador
| | - Alfeu de Medeiros Fleck Jr
- Liver Transplantation Group, Santa Casa de Misericórdia de Porto Alegre, Porto Alegre 90020090, RS, Brazil
| | - Claudio Augusto Marroni
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre 90050170, RS, Brazil
- Liver Transplantation Group, Santa Casa de Misericórdia de Porto Alegre, Porto Alegre 90020090, RS, Brazil
| | - Mário B Wagner
- School of Medicine, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre 90035002, RS, Brazil
| | - Alex Hörbe
- Interventional Radiology Unit, Santa Casa de Misericórdia de, Porto Alegre 90020090, RS, Brazil
| | - Matheus V Fernandes
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre 90050170, RS, Brazil
| | - Carlos TS Cerski
- Department of Pathology, School of Medicine, Universidade Federal do Rio Grande do Sul, Porto Alegre 90035002, RS, Brazil
| | - Gabriela Perdomo Coral
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre 90050170, RS, Brazil
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Zhou YW, Li QF, Chen YY, Wang K, Pu D, Chen XR, Li CH, Jiang L, Wang Y, Li Q, Yang Y, Gou HF, Bi F, Liu JY, Chen Y, Qiu M. Clinicopathologic features, treatment, survival, and prognostic factors of combined hepatocellular and cholangiocarcinoma: A nomogram development based on SEER database and validation in multicenter study. EUROPEAN JOURNAL OF SURGICAL ONCOLOGY 2022; 48:1559-1566. [PMID: 35115213 DOI: 10.1016/j.ejso.2022.01.023] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/05/2021] [Revised: 10/07/2021] [Accepted: 01/23/2022] [Indexed: 02/05/2023]
Abstract
PURPOSE The aim of the study was to comprehensively understand the combined hepatocellular and cholangiocarcinoma (CHC) and develop a nomogram for prognostic prediction of CHC. METHODS Data were collected from the Surveillance, Epidemiology and End Results (SEER) database (year 2004-2014). Propensity-score matching (PSM) was used to match the demographic characteristic of the CHC versus hepatocellular carcinoma (HCC) and intrahepatic cholangiocarcinoma (ICC). A nomogram model was established to predict the prognosis in terms of cancer specific survival (CSS). The established nomogram was externally validated by a multicenter cohort. RESULTS A total of 71,756 patients enrolled in our study including 62,877 HCC patients, 566 CHC patients, and 8303 ICC patients. The CHC, HCC, and ICC are not exactly similar in clinical characteristic. After PSM, the CSS of CHC was better than HCC but comparable to ICC. Tumor size, M stage, surgery, chemotherapy, and surgery were independently prognostic factors of CHC and were included in the establishment of novel nomogram. The c-index of the novel nomogram in SEER training set and multicenter validation was 0.779 and 0.780, respectively, which indicated that the model was with better discrimination power. In addition, decision curve analyses proved the favorable potential clinical effect of the predictive model. Lastly, a risk classification based on nomogram also verified the reliability of the model. CONCLUSION CHC had better survival than HCC but was comparable to ICC. The nomogram was established based on tumor size, M stage, chemotherapy, surgery, and radiotherapy and well validated by external multicenter cohort.
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Affiliation(s)
- Yu-Wen Zhou
- Department of Biotherapy, Cancer Center, West China Hospital of Sichuan University, Chengdu, China; Key Laboratory of Biotherapy, Cancer Center, West China Hospital, Sichuan University, China
| | - Qing-Fang Li
- Department of Biotherapy, Cancer Center, West China Hospital of Sichuan University, Chengdu, China; Key Laboratory of Biotherapy, Cancer Center, West China Hospital, Sichuan University, China
| | - Yue-Yun Chen
- Department of Biotherapy, Cancer Center, West China Hospital of Sichuan University, Chengdu, China; Key Laboratory of Biotherapy, Cancer Center, West China Hospital, Sichuan University, China
| | - Kai Wang
- Institute for Emergency Medicine and Disaster Medicine, Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China, China
| | - Dan Pu
- Lung Cancer Center, West China Hospital, Sichuan University, Chengdu, China
| | - Xiao-Rong Chen
- Department of Abdominal Oncology, Cancer Center, West China Hospital of Sichuan University, Chengdu, China
| | - Chun-Hong Li
- Department of Oncology, Suining Central Hospital, Suining, China
| | - Li Jiang
- Department of Abdominal Oncology, Sichuan Cancer Hospital, Chengdu, China
| | - Yan Wang
- Department of Oncology, The First People's Hospital of Long Quan Yi District, Chengdu, China
| | - Qiu Li
- Department of Abdominal Oncology, Cancer Center, West China Hospital of Sichuan University, Chengdu, China
| | - Yu Yang
- Department of Abdominal Oncology, Cancer Center, West China Hospital of Sichuan University, Chengdu, China
| | - Hong-Feng Gou
- Department of Abdominal Oncology, Cancer Center, West China Hospital of Sichuan University, Chengdu, China
| | - Feng Bi
- Department of Abdominal Oncology, Cancer Center, West China Hospital of Sichuan University, Chengdu, China
| | - Ji-Yan Liu
- Department of Biotherapy, Cancer Center, West China Hospital of Sichuan University, Chengdu, China; Key Laboratory of Biotherapy, Cancer Center, West China Hospital, Sichuan University, China.
| | - Ye Chen
- Department of Abdominal Oncology, Cancer Center, West China Hospital of Sichuan University, Chengdu, China.
| | - Meng Qiu
- Department of Abdominal Oncology, Cancer Center, West China Hospital of Sichuan University, Chengdu, China.
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7
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Fox AN, Liapakis A, Batra R, Bittermann T, Emamaullee J, Emre S, Genyk Y, Han H, Jackson W, Pomfret E, Raza M, Rodriguez-Davalos M, Rubman Gold S, Samstein B, Shenoy A, Taner T, Roberts JP. The use of nondirected donor organs in living donor liver transplantation: Perspectives and guidance. Hepatology 2022; 75:1579-1589. [PMID: 34859474 DOI: 10.1002/hep.32260] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/27/2021] [Revised: 11/04/2021] [Accepted: 11/05/2021] [Indexed: 12/13/2022]
Abstract
Interest in anonymous nondirected living organ donation is increasing in the United States and a small number of transplantation centers are accumulating an experience regarding nondirected donation in living donor liver transplantation. Herein, we review current transplant policy, discuss emerging data, draw parallels from nondirected kidney donation, and examine relevant considerations in nondirected living liver donation. We aim to provide a consensus guidance to ensure safe evaluation and selection of nondirected living liver donors and a schema for just allocation of nondirected grafts.
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Affiliation(s)
- Alyson N Fox
- Columbia University Irving Medical Center (CUIMC) Center for Liver Disease and Transplanation NY Presbyterian HospitalColumbia University Vagelos College of Physicians and SurgeonsNew YorkNew YorkUSA
| | - AnnMarie Liapakis
- Yale-New Haven Health Transplanation CenterYale University School of MedicineNew HavenConnecticutUSA
| | - Ramesh Batra
- Yale-New Haven Health Transplanation CenterYale University School of MedicineNew HavenConnecticutUSA
| | - Therese Bittermann
- Penn Transplant InstitutePenn MedicinePerelman School of Medicine Unniversity of PennsylvaniaPhiladelphiaPennsylvaniaUSA
| | - Juliet Emamaullee
- University of Southern California (USC) Transplant InstituteKeck School of Medicine of USCLos AngelesCaliforniaUSA
| | - Sukru Emre
- Yale-New Haven Health Transplanation CenterYale University School of MedicineNew HavenConnecticutUSA
| | - Yuri Genyk
- University of Southern California (USC) Transplant InstituteKeck School of Medicine of USCLos AngelesCaliforniaUSA
| | - Hyosun Han
- University of Southern California (USC) Transplant InstituteKeck School of Medicine of USCLos AngelesCaliforniaUSA
| | - Whitney Jackson
- Colorado Center for Transplantation Care, Research and EducationUniversity of Colorado School of MedicineAuroraColoradoUSA
| | - Elizabeth Pomfret
- Colorado Center for Transplantation Care, Research and EducationUniversity of Colorado School of MedicineAuroraColoradoUSA
| | - Muhammad Raza
- Keck School of Medicine of University of Southern CaliforniaLos AngelesCaliforniaUSA
| | | | - Susan Rubman Gold
- Yale-New Haven Health Transplanation CenterYale University School of MedicineNew HavenConnecticutUSA
| | - Benjamin Samstein
- Weill Cornell Medicine Center for Liver Disease and Transplantation NY Presbyterian HospitalWeill Cornell School of MedicineNew YorkNew YorkUSA
| | - Akhil Shenoy
- Columbia University Irving Medical Center (CUIMC) Center for Liver Disease and Transplanation NY Presbyterian HospitalColumbia University Vagelos College of Physicians and SurgeonsNew YorkNew YorkUSA
| | - Timucin Taner
- Mayo Clinic Transplant CenterMayo Clinic College of MedicineRochesterMinnesotaUSA
| | - John P Roberts
- Organ Transplant ProgramUniversity of California San Francisco (UCSF) HealthUCSF School of MedicineSan FranciscoCaliforniaUSA
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8
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Chen Y, Lu Q, Zhang W, Cao J, Dong Y, Wang W. Preoperative Differentiation of Combined Hepatocellular-Cholangiocarcinoma From Hepatocellular Carcinoma and Intrahepatic Cholangiocarcinoma: A Nomogram Based on Ultrasonographic Features and Clinical Indicators. Front Oncol 2022; 12:757774. [PMID: 35242699 PMCID: PMC8885729 DOI: 10.3389/fonc.2022.757774] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/12/2021] [Accepted: 01/24/2022] [Indexed: 11/13/2022] Open
Abstract
OBJECTIVE To establish a predictive nomogram to distinguish combined hepatocellular-cholangiocarcinoma (CHC) from hepatocellular carcinoma (HCC) and intrahepatic cholangiocarcinoma (ICC) based on preoperative clinical and ultrasound findings. METHODS A total of 261 patients with pathologically confirmed primary liver cancers (PLCs) were enrolled in this retrospective study, comprising 87 CHCs, 87 HCCs, and 87 ICCs matched by propensity score matching. Patients were randomly assigned to a training cohort and a validation one at the ratio of 7:3. A nomogram integrating ultrasound imaging characteristics and clinical features was established based on the independent risk factors selected by least absolute shrinkage and selection operator (LASSO) regression. The performance of the nomogram was evaluated in the training and validation cohorts in terms of discrimination, calibration, and clinical usefulness. RESULTS The nomogram, consisting of ultrasound imaging features (shape and margin on B-mode ultrasound, enhanced pattern on contrast-enhanced ultrasound) and clinical information [elevated alpha fetoprotein (AFP) level and serum protein electrophoresis (SPE) α1 level], showed promising performance in differentiating CHC from HCC and ICC, with the concordance index (C-index) of 0.8275 and 0.8530 in the training cohort and the validation cohort, respectively. Hosmer-Lemeshow test and the calibration curves suggested good consistency between predictions and observations. High clinical practicability was confirmed by the decision curve analysis. CONCLUSIONS The nomogram based on clinical and ultrasound imaging characteristics showed good performance in the discrimination of CHC from other subtypes of PLC and would be valuable in clinical decision-making.
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Affiliation(s)
- Yanling Chen
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
| | - Qing Lu
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
| | - Weibin Zhang
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
| | - Jiaying Cao
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
| | - Yi Dong
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
| | - Wenping Wang
- Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
- Shanghai Institute of Medical Imaging, Shanghai, China
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9
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Lin YC, Lin TS, Lin CC, Liu YW, Wang SH, Wu YJ, Li WF, Lin YH, Lin TL, Chan YC, Yeh CH, Wang CC, Chen CL, Yong CC. Can Microscopic Biliary Reconstruction Reduce Biliary Complication Rate in ABO-Incompatible Adult Living Donor Liver Transplantation? Ann Transplant 2021; 26:e931963. [PMID: 34446690 PMCID: PMC8406902 DOI: 10.12659/aot.931963] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/10/2023] Open
Abstract
Background With the introduction of rituximab, ABO-incompatible (ABOi) living donor liver transplantation (LDLT) has been considered a feasible and safe procedure to overcome the shortage of organ donors. However, higher biliary complication rates remain an unresolved problem in the ABOi group. In our center, biliary anastomosis has been done with microscopic biliary reconstruction (MBR), which effectively reduced the biliary complication rate. The aim of the current study was to investigate whether the microscopic approach reduced anastomotic biliary complications in ABOi LDLT. Material/Methods From March 2006 to December 2018, 30 adult ABOi and 60 ABO-compatible (ABOc) LDLT patients were selected from over 1300 recipients through 1: 2 propensity score-matched cohorts. All patients received MBR during the transplantation. Biliary complications included bile leakage and biliary stricture. Patients with diffuse intrahepatic biliary stricture were excluded from analysis. Results Patient characteristics were similar in the 2 groups. There was no in-hospital mortality in the ABOi LDLT. The long-term survival rates of the ABOi patients were comparable to those of the patients that underwent ABOc LDLT (87.1% vs 87.4%, P=0.964). Those in the ABOi group with anastomotic biliary complications were about 40%, which was higher than in the ABOc patients (40% vs 15%, P=0.01). Conclusions Microscopic biliary reconstruction does not help to reduce the high biliary complication rate in ABOi LDLT. Further investigation and identification regarding other risk factors and precautionary measures involving immunologic and adaptation mechanisms are needed.
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Affiliation(s)
- Yu-Cheng Lin
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Tsan-Shiun Lin
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Chih-Che Lin
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Yueh-Wei Liu
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Shih-Ho Wang
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Yi-Ju Wu
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Wei-Feng Li
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Yu-Hung Lin
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Ting-Lung Lin
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Yi-Chia Chan
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Cheng-Hsi Yeh
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Chih-Chi Wang
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Chao-Long Chen
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
| | - Chee-Chien Yong
- Liver Transplantation Center and Department of Surgery, Kaohsiung Chang Gung Memorial Hospital, and Chang Gung University College of Medicine, Kaohsiung, Taiwan
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10
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Jaradat D, Bagias G, Lorf T, Tokat Y, Obed A, Oezcelik A. Liver transplantation for combined hepatocellular-cholangiocarcinoma: Outcomes and prognostic factors for mortality. A multicenter analysis. Clin Transplant 2021; 35:e14094. [PMID: 32970878 DOI: 10.1111/ctr.14094] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/03/2020] [Revised: 08/06/2020] [Accepted: 09/07/2020] [Indexed: 12/12/2022]
Abstract
INTRODUCTION Combined hepatocellular-cholangiocarcinoma is rare and comprises features of hepatocellular carcinoma and cholangiocarcinoma. The treatment of choice has not yet been defined. The aim of the study was to analyze outcomes of patients with combined hepatocellular-cholangiocarcinoma, who underwent liver transplantation. MATERIAL AND METHODS All patients with combined hepatocellular-cholangiocarcinoma, who underwent liver transplantation, from January 2001 to August 2018 were identified. Pre-, intra- and postoperative data were retrospectively assessed. A univariate analysis was performed to identify prognostic factors. RESULTS A total number of 19 patients were included to this study. Perioperative death was seen in two patients (10.5%). Recurrent disease was reported in 11 patients (64.7%) within the median time of 4 months. One and three years survival rates were 57.1% (CI 0.301-1) and 38.1% (CI 0.137-1). Factors associated mortality were tumor size >3 cm, presence of lymphatic invasion, and prolonged ICU stay. Patients with mixed HCC-CC lesions have significantly better survival compared to patients with separate lesions of HCC and CCC in one liver (p = .025). CONCLUSION Although overall survival rates are clearly decreased compared to HCC patients, liver transplantation should be taken under consideration for selected patients with early stage and real mixed HCC-CC, who are likely to benefit from liver transplantation.
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Affiliation(s)
- Derar Jaradat
- Department of General, Visceral and Transplantation Surgery, University Hospital of Essen, Essen, Germany
| | - Georgios Bagias
- Department of General, Visceral and Transplantation Surgery, University Hospital of Essen, Essen, Germany
| | - Thomas Lorf
- Department of Surgery, University of Göttingen, Göttingen, Germany
| | - Yaman Tokat
- Department of General and Transplantation Surgery, Florence Nightingale Hospital, University Hospital of Istanbul Bilim University, Istanbul, Turkey
| | - Aiman Obed
- Department of Hepatobiliary and Organ Transplant Surgery, Hospital Jordan, Amman, Jordan
| | - Arzu Oezcelik
- Department of General, Visceral and Transplantation Surgery, University Hospital of Essen, Essen, Germany
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11
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Clinical features and outcomes of combined hepatocellular carcinoma and cholangiocarcinoma versus hepatocellular carcinoma versus cholangiocarcinoma after surgical resection: a propensity score matching analysis. BMC Gastroenterol 2021; 21:20. [PMID: 33413162 PMCID: PMC7788698 DOI: 10.1186/s12876-020-01586-4] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/03/2020] [Accepted: 12/16/2020] [Indexed: 02/06/2023] Open
Abstract
Background Combined hepatocellular carcinoma and cholangiocarcinoma (cHCC-CC) is an infrequent type of primary liver cancer that comprises hepatocellular carcinoma (HCC) and cholangiocarcinoma (CC). This study investigated the clinicopathological features and prognosis among cHCC-CC, HCC, and CC groups. Methods We prospectively collected the data of 608 patients who underwent surgical resection for liver cancer between 2011 and 2018 at E-Da Hospital, I-Shou University, Kaohsiung, Taiwan. Overall, 505 patients with cHCC-CC, HCC, and CC were included, and their clinicopathological features, overall survival (OS), and recurrence were recorded. OS and recurrence rates were analyzed using the Kaplan–Meier analysis. Results In the entire cohort, the median age was 61 years and 80% were men. Thirty-five (7.0%) had cHCC-CC, 419 (82.9%) had HCC, and 51 (10.1%) had CC. The clinicopathological features of the cHCC-CC group were more identical to those of the HCC group than the CC group. OS was significantly lower in the cHCC-CC group than in the HCC group but was not significantly higher in the cHCC-CC group than in the CC group. The median OS of cHCC-CC, HCC, and CC groups was 50.1 months [95% confidence interval (CI): 38.7–61.2], 62.3 months (CI: 42.1–72.9), and 36.2 months (CI: 15.4–56.5), respectively. Cumulative OS rates at 1, 3, and 5 years in cHCC-CC, HCC, and CC groups were 88.5%, 62.2%, and 44.0%; 91.2%, 76.1%, and 68.0%; and 72.0%, 48.1%, and 34.5%, respectively. After propensity score matching (PSM), OS in the cHCC-CC group was not significantly different from that in the HCC or CC group. However, OS was significantly higher in the HCC group than in the CC group before and after PSM. Furthermore, the disease-free survival was not significantly different among cHCC-CC, HCC, and CC groups before and after PSM. Conclusion The clinicopathological features of the cHCC-CC group were more identical to those of the HCC group than the CC group. The OS rate was significantly lower in the cHCC-CC group than the HCC group. However, after PSM, OS and disease-free survival in the cHCC-CC group were not significantly different from those in the HCC or CC group.
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12
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Tang Y, Wang L, Teng F, Zhang T, Zhao Y, Chen Z. The clinical characteristics and prognostic factors of combined Hepatocellular Carcinoma and Cholangiocarcinoma, Hepatocellular Carcinoma and Intrahepatic Cholangiocarcinoma after Surgical Resection: A propensity score matching analysis. Int J Med Sci 2021; 18:187-198. [PMID: 33390787 PMCID: PMC7738961 DOI: 10.7150/ijms.50883] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/20/2020] [Accepted: 10/13/2020] [Indexed: 02/05/2023] Open
Abstract
Background: Clinical characteristics and prognosis among combined hepatocellular carcinoma (HCC) and cholangiocarcinoma (cHCC-CC) with HCC and intrahepatic cholangiocarcinoma (ICC) were inconsistent in previous studies. The aim of this study was to compare postoperative prognosis among cHCC-CC, HCC and ICC, and investigated the prognostic risk factor of cHCC-CC after surgical resection. Methods: A total of 1041 eligible patients with pathological diagnosis of cHCC-CC (n=135), HCC (n=698) and ICC (n=208) were enrolled in this study. Univariate and multivariate Cox analysis were applied for assessing important risk factors. cHCC-CC were further 1:1 matched with HCC and ICC on important clinical risk factors. Survival curves of matched and unmatched cohorts were depicted by Kaplan-Meier method with log-rank test. Results: Patients with cHCC-CC had similar rate of sex, age and cirrhosis with HCC (p<0.05) and comparable incidence of hepatitis B or C with ICC (p=0.197). Patients of cHCC-CC had intermediate prognosis between HCC and ICC, with median overall survival (OS) time of cHCC-CC, HCC and ICC of 20.5 months, 35.7 months and 11.6 months (p<0.001). In matched cohorts, the OS of cHCC-CC were worse than HCC (p<0.001) but comparable with ICC (p=0.06), while the disease-free survival (DFS) of cHCC-CC was worse than HCC but better than ICC (p<0.05). And lymph node infiltration and postoperative transarterial chemoembolization (TACE) were independent risk factors of cHCC-CC associated with prognosis. Conclusion: The long term survival of cHCC-CC was worse than HCC but comparable with ICC when matched on albumin level, tumor size, lymph node infiltration, tumor stage and margin. Presence of lymph node infiltration and no postoperative TACE were associated with poor prognosis of cHCC-CC.
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Affiliation(s)
- Youyin Tang
- Department of Liver Surgery, Liver Transplantation Center, West China Hospital of Sichuan University, No. 37 GuoXue Alley, Chengdu 610041, P.R. China
| | - Lingyan Wang
- Department of Obstetrics and Gynecology Nursing, Key Laboratory of Birth Defects and Related Disease of Women and Children, West China Second University Hospital, Sichuan University, No. 20 South Renmin Road, Chengdu 610041, P.R. China
| | - Fei Teng
- Department of Liver Surgery, Liver Transplantation Center, West China Hospital of Sichuan University, No. 37 GuoXue Alley, Chengdu 610041, P.R. China
| | - Tao Zhang
- Department of Biotherapy, West China Hospital and State Key Laboratory of Biotherapy, Sichuan University, No. 37 GuoXue Alley, Chengdu 610041, P.R. China
| | - Yunuo Zhao
- Department of Biotherapy, West China Hospital and State Key Laboratory of Biotherapy, Sichuan University, No. 37 GuoXue Alley, Chengdu 610041, P.R. China
| | - Zheyu Chen
- Department of Liver Surgery, Liver Transplantation Center, West China Hospital of Sichuan University, No. 37 GuoXue Alley, Chengdu 610041, P.R. China
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13
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Razik A, Malla S, Goyal A, Gamanagatti S, Kandasamy D, Das CJ, Sharma R, Gupta AK. Unusual Primary Neoplasms of the Adult Liver: Review of Imaging Appearances and Differential Diagnosis. Curr Probl Diagn Radiol 2020; 51:73-85. [PMID: 33199074 DOI: 10.1067/j.cpradiol.2020.10.001] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/16/2020] [Accepted: 10/16/2020] [Indexed: 12/24/2022]
Abstract
The radiological appearance of common primary hepatic tumors such as hepatocellular carcinoma (HCC) and cholangiocarcinoma (CCA) is widely recognized. Hepatic masses with unusual histology are occasionally encountered, but seldom suspected on imaging. However, many possess characteristic imaging findings, which when assessed along with the clinical and demographic background and serum tumor markers, may enable a prospective diagnosis. This review attempts to familiarize the reader with the clinicopathological characteristics, imaging manifestations, and differential diagnosis of these unusual liver tumors in adults. Biphenotypic primary liver carcinoma is suspected in masses showing distinct areas of HCC and CCA-type enhancement pattern in cirrhotic livers. Fibrolamellar carcinoma occurs in young individuals without underlying chronic liver disease and shows a characteristic T2-hypointense scar frequently showing calcification. Perivascular epithelioid cell tumors are differentials for any arterial hyperenhancing mass in the noncirrhotic liver, particularly in patients with tuberous sclerosis. Multifocal subcapsular tumors showing target-like morphology, capsular retraction and "lollipop" sign are suspicious for epithelioid hemangioendothelioma. On the other hand, multiple hemorrhagic lesions showing patchy areas of bizarre-shaped arterial phase hyperenhancement are suspicious for angiosarcoma. Primary hepatic lymphoma (PHL) is suspected when patients with immunosuppression present with solitary or multifocal masses that insinuate around vessels and bile ducts without causing luminal narrowing. Intense diffusion restriction and low-level homogeneous or target-like enhancement are also ancillary features of PHL. Primary hepatic neuroendocrine tumor shows uptake on Ga-68 DOTANOC PET/CT. Although a straightforward diagnosis may be difficult in these cases, awareness of the characteristic imaging appearances is helpful in suspecting the diagnosis.
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Affiliation(s)
- Abdul Razik
- Department of Radiodiagnosis, All India Institute of Medical Sciences (A.I.I.M.S), New Delhi, India
| | - Sundeep Malla
- Department of Radiodiagnosis, All India Institute of Medical Sciences (A.I.I.M.S), New Delhi, India
| | - Ankur Goyal
- Department of Radiodiagnosis, All India Institute of Medical Sciences (A.I.I.M.S), New Delhi, India
| | - Shivanand Gamanagatti
- Department of Radiodiagnosis, All India Institute of Medical Sciences (A.I.I.M.S), New Delhi, India
| | | | - Chandan Jyoti Das
- Department of Radiodiagnosis, All India Institute of Medical Sciences (A.I.I.M.S), New Delhi, India
| | - Raju Sharma
- Department of Radiodiagnosis, All India Institute of Medical Sciences (A.I.I.M.S), New Delhi, India.
| | - Arun Kumar Gupta
- Department of Radiodiagnosis, All India Institute of Medical Sciences (A.I.I.M.S), New Delhi, India
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14
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Takamura H, Gabata R, Obatake Y, Nakanuma S, Hayashi H, Kozaka K, Sasaki M, Okazaki M, Yamaguchi T, Shimbashi H, Terai S, Okamoto K, Makino I, Kinoshita J, Nakamura K, Miyashita T, Tajima H, Ninomiya I, Fushida S, Kitao A, Kitahara M, Arai K, Yamashita T, Yamashita T, Ikeda H, Satoh Y, Harada K, Kaneko S, Gabata T, Kosaka T, Ohta T. Clinical features and diagnostic imaging of cholangiolocellular carcinoma compared with other primary liver cancers: a surgical perspective. Technol Cancer Res Treat 2020; 19:1533033820948141. [PMID: 33073719 PMCID: PMC7592326 DOI: 10.1177/1533033820948141] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/23/2022] Open
Abstract
Background and Objectives: Although cholangiolocellular carcinoma is considered a combined hepatocellular and cholangiocarcinoma, we feel that this classification is not appropriate. Therefore, we compared the diagnostic imaging findings, surgical prognosis, and pathological features of cholangiolocellular carcinoma with those of other combined hepatocellular and cholangiocarcinoma subtypes, hepatocellular carcinoma, and cholangiocarcinoma. Methods: The study patients included 7 with classical type combined hepatocellular and cholangiocarcinoma; 8 with stem cell feature, intermediate type combined hepatocellular and cholangiocarcinoma; 13 with cholangiolocellular carcinoma; 58 with cholangiocarcinoma; and 359 with hepatocellular carcinoma. All patients underwent hepatectomy or living-related donor liver transplantation from 2001 to 2014. Results: cholangiolocellular carcinoma could be distinguished from hepatocellular carcinom, other combined hepatocellular and cholangiocarcinoma subtypes, and cholangiocarcinoma by the presence of intratumoral Glisson’s pedicle, hepatic vein penetration, and tumor-staining pattern on angiography-assisted CT. Cholangiolocellular carcinoma was associated with a significantly lower SUV-max than that of cholangiocarcinoma on FDG-PET. Hepatocellular carcinoma, classical type, and cholangiolocellular carcinoma had significantly better prognoses than stem cell feature, intermediate type and cholangiocarcinoma. A cholangiocarcinoma component was detected in cholangiolocellular carcinoma that progressed to the hepatic hilum, and the cholangiocarcinoma component was found in perineural invasion and lymph node metastases. Conclusions: From the viewpoint of surgeon, cholangiolocellular carcinoma should be classified as a good-prognosis subtype of biliary tract carcinoma because of its tendency to differentiate into cholangiocarcinoma during its progression, and its distinctive imaging and few recurrence rates different from other combined hepatocellular and cholangiocarcinoma subtypes.
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Affiliation(s)
- Hiroyuki Takamura
- General and Digestive Surgery, 12857Kanazawa Medical University, Kahoku, Ishikawa, Japan.,Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Ryousuke Gabata
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Yoshinao Obatake
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Shinichi Nakanuma
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Hironori Hayashi
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Kazuto Kozaka
- Radiology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Motoko Sasaki
- Pathology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Mitsuyoshi Okazaki
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Takahisa Yamaguchi
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Hiroyuki Shimbashi
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Shiro Terai
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Koichi Okamoto
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Isamu Makino
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Jun Kinoshita
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Keishi Nakamura
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Tomoharu Miyashita
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Hidehiro Tajima
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Itasu Ninomiya
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Sachio Fushida
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Azusa Kitao
- Radiology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Masaaki Kitahara
- Gastroenterology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Kuniaki Arai
- Gastroenterology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Taro Yamashita
- Gastroenterology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Tatsuya Yamashita
- Gastroenterology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Hiroko Ikeda
- Pathology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Yasunori Satoh
- Pathology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Kenichi Harada
- Pathology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | - Syuichi Kaneko
- Gastroenterology, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
| | | | - Tateo Kosaka
- General and Digestive Surgery, 12857Kanazawa Medical University, Kahoku, Ishikawa, Japan
| | - Tetsuo Ohta
- Gastroenterologic Surgery, 12858Kanazawa University, Kanazawa, Ishikawa, Japan
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15
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Peng Y, Lin P, Wu L, Wan D, Zhao Y, Liang L, Ma X, Qin H, Liu Y, Li X, Wang X, He Y, Yang H. Ultrasound-Based Radiomics Analysis for Preoperatively Predicting Different Histopathological Subtypes of Primary Liver Cancer. Front Oncol 2020; 10:1646. [PMID: 33072550 PMCID: PMC7543652 DOI: 10.3389/fonc.2020.01646] [Citation(s) in RCA: 40] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/14/2020] [Accepted: 07/27/2020] [Indexed: 12/12/2022] Open
Abstract
Background Preoperative identification of hepatocellular carcinoma (HCC), combined hepatocellular–cholangiocarcinoma (cHCC-ICC), and intrahepatic cholangiocarcinoma (ICC) is essential for treatment decision making. We aimed to use ultrasound-based radiomics analysis to non-invasively distinguish histopathological subtypes of primary liver cancer (PLC) before surgery. Methods We retrospectively analyzed ultrasound images of 668 PLC patients, comprising 531 HCC patients, 48 cHCC-ICC patients, and 89 ICC patients. The boundary of a tumor was manually determined on the largest imaging slice of the ultrasound medicine image by ITK-SNAP software (version 3.8.0), and then, the high-throughput radiomics features were extracted from the obtained region of interest (ROI) of the tumor. The combination of different dimension-reduction technologies and machine learning approaches was used to identify important features and develop the moderate radiomics model. The comprehensive ability of the radiomics model can be evaluated by the area under the receiver operating characteristic curve (AUC). Results After digitally processing tumor ultrasound images, 5,234 high-throughput radiomics features were obtained. We used the Spearman + least absolute shrinkage and selection operator (LASSO) regression method for feature selection and logistics regression for modeling to develop the HCC-vs-non-HCC radiomics model (composed of 16 features). The Spearman + statistical test + random forest methods were used for feature selection, and logistics regression was applied for modeling to develop the ICC-vs-cHCC-ICC radiomics model (composed of 19 features). The overall performance of the radiomics model in identifying different histopathological types of PLC was moderate, with AUC values of 0.854 (training cohort) and 0.775 (test cohort) in the HCC-vs-non-HCC radiomics model and 0.920 (training cohort) and 0.728 (test cohort) in the ICC-vs-cHCC-ICC radiomics model. Conclusion Ultrasound-based radiomics models can help distinguish histopathological subtypes of PLC and provide effective clinical decision making for the accurate diagnosis and treatment of PLC.
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Affiliation(s)
- Yuting Peng
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Peng Lin
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Linyong Wu
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Da Wan
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Yujia Zhao
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Li Liang
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Xiaoyu Ma
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Hui Qin
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Yichen Liu
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Xin Li
- GE Healthcare, Shanghai, China
| | | | - Yun He
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
| | - Hong Yang
- Department of Medical Ultrasonics, The First Affiliated Hospital of Guangxi Medical University, Nanning, China
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16
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Ito T, Ishii T, Sumiyoshi S, Ogiso S, Fukumitsu K, Ito T, Yagi S, Seo S, Hata K, Taura K, Uemoto S. Living donor liver transplantation for combined hepatocellular-cholangiocarcinoma: A case series of four patients. Int J Surg Case Rep 2020; 74:46-52. [PMID: 32791447 PMCID: PMC7424173 DOI: 10.1016/j.ijscr.2020.07.069] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2020] [Revised: 07/14/2020] [Accepted: 07/21/2020] [Indexed: 02/07/2023] Open
Abstract
Combined hepatocellular-cholangiocarcinoma (cHCC-CCA) is a rare primary liver carcinoma. The indications for live transplantation for cHCC-CCA remain controversial. In this case series, patients who met the Milan criteria on the pathological examination had good prognosis. By itself, cHCC-CCA was not a contraindication for liver transplantation. Introduction Combined hepatocellular-cholangiocarcinoma (cHCC-CCA) is a rare primary liver carcinoma whose components include both hepatocellular carcinoma (HCC) and cholangiocarcinoma (CCA). Indications for liver transplantation for cHCC-CCA remain controversial. Case presentations Four patients underwent living donor liver transplantation (LDLT) for cHCC-CCA. All patients had multiple tumor nodules preoperatively diagnosed as HCC. Postoperative pathological examinations revealed that one of the tumors was cHCC-CCA. Cases 1 and 2 underwent LDLT for cirrhosis with HCC tumors that met Milan criteria. Case 3 underwent LDLT for recurrent HCC tumors with nonalcoholic steatohepatitis. Although the preoperative examinations showed that the patient met the Kyoto, but not Milan criteria, postoperative pathological examinations revealed that the patient did meet Milan criteria. The three patients who met Milan criteria on postoperative pathological examination had no recurrences after LDLT. Case 4 had multiple tumors with alcoholic liver cirrhosis. Although the preoperative examinations showed that the patient did not meet Milan criteria—but did meet Kyoto criteria—, on postoperative pathological examinations, the patient met neither Millan nor Kyoto criteria. He died of tumor recurrence 15 months after LDLT. Discussion and conclusions Our experiences suggested that patients who meet Millan or Kyoto criteria experienced acceptable outcomes of LDLT for cHCC-CCA. By itself, cHCC-CCA is not contraindication for liver transplantation.
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Affiliation(s)
- Takashi Ito
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Takamichi Ishii
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan.
| | - Shinji Sumiyoshi
- Department of Diagnostic Pathology, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Satoshi Ogiso
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Ken Fukumitsu
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Takashi Ito
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Shintaro Yagi
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Satoru Seo
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Koichiro Hata
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Kojiro Taura
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
| | - Shinji Uemoto
- Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan
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17
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Hafeez Bhatti AB, Tahir R, Qureshi NR, Mamoon N, Khan NY, Zia HH. Living donor liver transplantation for intra hepatic cholangiocarcinoma. Ann Med Surg (Lond) 2020; 57:82-84. [PMID: 32728435 PMCID: PMC7381427 DOI: 10.1016/j.amsu.2020.07.028] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/19/2020] [Accepted: 07/11/2020] [Indexed: 12/21/2022] Open
Affiliation(s)
- Abu Bakar Hafeez Bhatti
- Department of HPB Surgery and Liver Transplantation, Shifa International Hospital, Islamabad, Pakistan
| | - Rizmi Tahir
- Department of HPB Surgery and Liver Transplantation, Shifa International Hospital, Islamabad, Pakistan
| | - Najla Rahman Qureshi
- Department of HPB Surgery and Liver Transplantation, Shifa International Hospital, Islamabad, Pakistan
| | - Nadira Mamoon
- Department of Pathology, Shifa International Hospital, Islamabad, Pakistan
| | - Nusrat Yar Khan
- Department of HPB Surgery and Liver Transplantation, Shifa International Hospital, Islamabad, Pakistan
| | - Haseeb Haider Zia
- Department of HPB Surgery and Liver Transplantation, Shifa International Hospital, Islamabad, Pakistan
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Gentile D, Donadon M, Lleo A, Aghemo A, Roncalli M, di Tommaso L, Torzilli G. Surgical Treatment of Hepatocholangiocarcinoma: A Systematic Review. Liver Cancer 2020; 9:15-27. [PMID: 32071906 PMCID: PMC7024854 DOI: 10.1159/000503719] [Citation(s) in RCA: 62] [Impact Index Per Article: 12.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/20/2019] [Accepted: 09/13/2019] [Indexed: 02/04/2023] Open
Abstract
BACKGROUND Hepatocholangiocarcinoma (HCC-CC) is a rare liver malignancy that contains features of both hepatocellular carcinoma (HCC) and mass-forming cholangiocarcinoma (MFCCC). Three classification systems for HCC-CC are described in literature and the majority of these tumors appear to be of the transitional type. The aim of this study is to evaluate the characteristics of transitional HCC-CC and to compare long-term oncological outcomes with HCC and MFCCC in surgically treated patients. SUMMARY A systematic literature search was conducted to identify relevant studies analyzing demographic and clinical characteristics of patients with transitional HCC-CC and evaluating treatments and outcomes associated with this neoplasm. Only comparative, retrospective analyses were included. A total of 14 studies, involving 13,613 patients with primary liver malignancy, were analyzed. All patients underwent surgery, either liver resection or transplantation. Four hundred and thirty-seven patients were affected by transitional HCC-CC (3.2%). For further analysis, patients with transitional HCC-CC were divided into 2 groups, the resection group and the transplantation group. Disease-free survival (DFS) and overall survival (OS) of these patients were analyzed and compared to long-term oncological outcomes of patients with HCC and/or MFCCC, who underwent the same treatment. In the resection group, DFS rate at 5-year was 15, 31.6, and 20.3% for patients with transitional HCC-CC, HCC, and MFCCC, respectively; OS rate at 5-year was 32.7, 47.5, and 30.3% for patients with transitional HCC-CC, HCC, and MFCCC, respectively. In the transplantation group, DFS rate at 5-year was 40.9 and 87.4% for patients with transitional HCC-CC and HCC, respectively; OS rate at 5-year was 49.4 and 80.3% for patients with transitional HCC-CC and HCC, respectively. KEY MESSAGES Transitional HCC-CC patients have significantly worse DFS and OS rates compared to HCC patients in both the resection group and the transplantation group. However, in the resection group, both DFS and OS rates of transitional HCC-CC patients are not statistically different from those of MFCCC patients.
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Affiliation(s)
- Damiano Gentile
- aDepartment of Hepatobiliary and General Surgery, Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano, Milan, Italy
| | - Matteo Donadon
- aDepartment of Hepatobiliary and General Surgery, Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano, Milan, Italy
| | - Ana Lleo
- bDepartment of Internal Medicine and Hepatology, Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano, Milan, Italy
| | - Alessio Aghemo
- bDepartment of Internal Medicine and Hepatology, Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano, Milan, Italy
| | - Massimo Roncalli
- cDepartment of Pathology, Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano, Milan, Italy
| | - Luca di Tommaso
- cDepartment of Pathology, Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano, Milan, Italy
| | - Guido Torzilli
- aDepartment of Hepatobiliary and General Surgery, Humanitas University, Humanitas Clinical and Research Center, IRCCS, Rozzano, Milan, Italy
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Liver transplantation for unresectable malignancies: Beyond hepatocellular carcinoma. Eur J Surg Oncol 2019; 45:2268-2278. [PMID: 31387755 DOI: 10.1016/j.ejso.2019.07.024] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/03/2019] [Revised: 07/02/2019] [Accepted: 07/18/2019] [Indexed: 12/12/2022] Open
Abstract
Indications for liver transplantation have expanded over the past few decades owing to improved outcomes and better understanding of underlying pathologies. In particular, there has been a growing interest in the field of transplant oncology in recent years that has led to considerable developments which have pushed the boundaries of malignant indications for liver transplantation beyond hepatocellular carcinoma (HCC). In this article, we review and summarise the published evidence for liver transplantation in non-HCC primary and metastatic liver malignancies and highlight ongoing clinical trials that address unresolved questions therein. We also examine the current technical, immunological and oncological challenges that face liver transplantation in this growing field and explore potential approaches to overcome these barriers.
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Mixed Hepatocellular Cholangiocarcinoma: A Review of Long-Term Outcomes Following Liver Transplantation. Transplant Proc 2019; 51:437-439. [PMID: 30879560 DOI: 10.1016/j.transproceed.2019.01.073] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/30/2022]
Abstract
INTRODUCTION Mixed hepatocellular cholangiocarcinoma (HCC-CC) represents a rare hepatic tumor, which demonstrates histological features of both hepatocellular carcinoma (HCC) and cholangiocarcinoma (CC). HCC-CC can be an unexpected finding in patients undergoing liver transplantation (LT) for HCC. The objective of our review was to review and evaluate long-term outcomes in patients undergoing LT for mixed HCC-CC. METHODS A meticulous MEDLINE search was performed for articles referring to long-term results in patients who underwent LT and whose final pathology revealed HCC-CC. RESULTS A total of 7 studies, which comprised 93 patients who underwent LT and whose resected specimen revealed mixed HCC-CC, were included in our review. One-year overall survival (OS) rates ranged from 64% to 93%, 3-year OS ranged from 38% to 78%, and 5-year OS rates range from 14% to 78%. Disease-free-survival (DFS) rates at 1-year from LT ranged from 60-% to 64%, whereas both 3- and 5-year DFS rates ranged from 30% to 53.3%. CONCLUSIONS Long-term results of LT in the setting of mixed HCC-CC are associated with fairly unfavorable overall outcomes compared to LT for other indications including HCC yet are improved compared to others such as intrahepatic CC. A stricter preoperative evaluation could potentially help identify the patients with mixed HCC-CC who are at high-risk after LT, reduce the risks of recurrence, and improve OS.
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Jeon SK, Joo I, Lee DH, Lee SM, Kang HJ, Lee KB, Lee JM. Combined hepatocellular cholangiocarcinoma: LI-RADS v2017 categorisation for differential diagnosis and prognostication on gadoxetic acid-enhanced MR imaging. Eur Radiol 2018; 29:373-382. [PMID: 29955948 DOI: 10.1007/s00330-018-5605-x] [Citation(s) in RCA: 94] [Impact Index Per Article: 13.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/02/2018] [Revised: 06/01/2018] [Accepted: 06/07/2018] [Indexed: 12/12/2022]
Abstract
OBJECTIVES To investigate the performance of the Liver Imaging Reporting and Data System (LI-RADS) v2017 for combined hepatocellular cholangiocarcinoma (cHCC-CCA) in the differential diagnosis from hepatocellular carcinoma (HCC) and prediction of prognosis on gadoxetic acid-enhanced MRI (Gd-EOB-MRI). METHODS Patients at high risk of HCC with pathologically confirmed cHCC-CCAs (n = 70) and a matched control of HCCs (n = 70) who had undergone Gd-EOB-MRI were included. LI-RADS category was assigned for each lesion by two radiologists. Imaging features and surgical outcomes were compared between cHCC-CCAs of LR-M and LR-5/4 using the χ2 test or Fisher's exact test. Recurrence-free survival (RFS) was estimated using Kaplan-Meier survival curves and compared using the log-rank test. RESULTS cHCC-CCAs and HCCs were categorised as LR-M, LR-5/4 and LR-TIV in 61.4% (43/70), 37.1% (26/70) and 1.4% (1/70) and 10.0% (7/70), 88.6% (62/70) and 1.4% (1/70), respectively. cHCC-CCAs of LR-5/4, in comparison to LR-M, showed significantly higher frequencies of major HCC features: arterial hyperenhancement (96.2% (25/26) vs. 58.1% (25/43), p = 0.001), washout appearance (80.8% (21/26) vs. 48.8% (21/43), p = 0.011) and enhancing capsule (34.6% (9/26) vs. 11.6% (5/43), p = 0.031). After curative surgery, patients with cHCC-CCAs of LR-M showed a higher early recurrence rate (≤ 6 months) than did those with LR-5/4 (27.8% (10/36) vs. 4.8% (1/21), p = 0.041), whereas no significant difference was observed in RFS (log-rank p = 0.084). CONCLUSIONS By using LI-RADS on Gd-EOB-MRI, a substantial proportion of cHCC-CCAs can be categorised as non-LR-M. In addition, cHCC-CCAs mimicking HCCs on imaging (LR-5/4) may indicate better surgical outcomes with regard to early recurrence than those of LR-M. KEY POINTS • cHCC-CCAs can be categorised as either LR-M or non-LR-M on Gd-EOB-MRI. • cHCC-CCAs of LR-5/4 frequently demonstrate major HCC imaging features. • LI-RADS categorisation may provide prognostic information after surgery in cHCC-CCAs.
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Affiliation(s)
- Sun Kyung Jeon
- Department of Radiology, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
- Department of Radiology, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
| | - Ijin Joo
- Department of Radiology, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea.
- Department of Radiology, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea.
| | - Dong Ho Lee
- Department of Radiology, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
- Department of Radiology, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
| | - Sang Min Lee
- Department of Radiology, Hallym University Sacred Heart Hospital, Anyang, Korea
| | - Hyo-Jin Kang
- Department of Radiology, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
- Department of Radiology, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
| | - Kyoung-Bun Lee
- Department of Pathology, Seoul National University Hospital, Seoul, Korea
| | - Jeong Min Lee
- Department of Radiology, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
- Department of Radiology, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea
- Institute of Radiation Medicine, Seoul National University Medical Research Center, Seoul, Korea
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